Diversity of Magneto-Aerotactic Behaviors and Oxygen Sensing Mechanisms in Cultured Magnetotactic Bacteria

Abstract

Microorganisms living in gradient environments affect large-scale processes, including the cycling of elements such as carbon, nitrogen or sulfur, the rates and fate of primary production, and the generation of climatically active gases. Aerotaxis is a common adaptation in organisms living in the oxygen gradients of stratified environments. Magnetotactic bacteria are such gradient-inhabiting organisms that have a specific type of aerotaxis that allows them to compete at the oxic-anoxic interface. They biomineralize magnetosomes, intracellular membrane-coated magnetic nanoparticles, that comprise a permanent magnetic dipole that causes the cells to align along magnetic field lines. The magnetic alignment enables them to efficiently migrate toward an optimal oxygen concentration in microaerobic niches. This phenomenon is known as magneto-aerotaxis. Magneto-aerotaxis has only been characterized in a limited number of available cultured strains. In this work, we characterize the magneto-aerotactic behavior of 12 magnetotactic bacteria with various morphologies, phylogenies, physiologies, and flagellar apparatus. We report six different magneto-aerotactic behaviors that can be described as a combination of three distinct mechanisms, including the reported (di-)polar, axial, and a previously undescribed mechanism we named unipolar. We implement a model suggesting that the three magneto-aerotactic mechanisms are related to distinct oxygen sensing mechanisms that regulate the direction of cells' motility in an oxygen gradient.

Constant Flux of Spatial Niche Partitioning through High-Resolution Sampling of Magnetotactic Bacteria

“…Oxygen concentration. Magnetotactic bacteria are microaerophilic and sensitive to O 2 ; thus, they prefer to live near the oxic-anoxic interface in sediments where O 2 levels are low (44). For this reason, O 2 profiles were measured at nine locations in each aquarium by using a Unisense OX50 oxygen microsensor (tip diameter of 50 m) with a 0.3-mol/liter detection limit on day 120.…”

Magnetotactic bacteria

“…While the best studied magnetotactic bacteria have magnetite (Fe 3 O 4 ) nanoparticles [6], some species have been found to use greigite (Fe 3 S 4 ) instead [12]. Likewise, the motility apparatus can display various organizations such as a single flagellum or a bundle of flagella at one pole or two flagella at opposite poles [13]. Furthermore, flagella can have different organizations with respect to the magnetosome chain.…”

“…grow best under conditions of low (but non-zero) oxygen concentration [39]. The preferred oxygen concentrations for magnetotactic bacteria are in the range of a 1-20 μM, low compared to a saturation concentration of oxygen in water of 216 μM [13]. Indeed, their natural habitat is the oxic-anoxic transition zone in layered aquatic environments, an area of great ecological diversity, which is typically located in the upper region of the sediment (mud) at the bottom of the water column [40].…”

“…For a magnetic field pointing towards the closed end of the capillary (the anoxic side), the oxygen gradient is antiparallel to the magnetic field as in the natural habitats on the Northern hemisphere. Magnetotactic bacteria form a band in such a situation [13,[41][42][43], i.e. a region of high bacterial density at a position where the local oxygen concentration corresponds to the preferred concentration.…”

Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions

“…Here, we show that the magneto-aerotactic migration behaviour 2 of magnetotactic bacteria 3 , Magnetococcus marinus strain MC-1 4 , can be used to transport drug-loaded nanoliposomes into hypoxic regions of the tumour. In their natural environment, MC-1 cells, each containing a chain of magnetic iron-oxide nanocrystals 5 , tend to swim along local magnetic field lines and towards low oxygen concentrations 6 based on a two-state aerotactic sensing system 2 . We show that when MC-1 cells bearing covalently bound drug-containing nanoliposomes were injected near the tumour in SCID Beige mice and magnetically guided, up to 55% of MC-1 cells penetrated into hypoxic regions of HCT116 colorectal xenografts.…”